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Journal of Clinical Oncology, Vol 26, No 27 (September 20), 2008: pp. 4480-4487 © 2008 American Society of Clinical Oncology. DOI: 10.1200/JCO.2007.15.7917 Prospective Relationships of Physical Activity With Quality of Life Among Colorectal Cancer Survivors
From the Viertel Centre for Research in Cancer Control, The Cancer Council Queensland, and the Cancer Prevention Research Centre, School of Population Health, University of Queensland, Brisbane, Australia; Institute of Human Performance, University of Hong Kong, Hong Kong; and the Children's Nutrition Research Center, Baylor College of Medicine, Houston, TX Corresponding author: Brigid M. Lynch, PhD, Viertel Centre for Research in Cancer Control, The Cancer Council Queensland, 553 Gregory Terrace, Fortitude Valley 4006, Australia; e-mail: brigidlynch{at}cancerqld.org.au
Purpose Physical activity can enhance quality of life for cancer survivors. However, few longitudinal studies have examined whether physical activity has a sustained effect on improvements in quality of life. The present study aims to examine the relationships between physical activity and quality of life over 2 years after a colorectal cancer diagnosis. Patients and Methods Data were collected within the Colorectal Cancer and Quality of Life Study, in which 1,966 people diagnosed with colorectal cancer were recruited through the Queensland Cancer Registry. Participants completed telephone interviews at approximately 6, 12, and 24 months after diagnosis. Generalized linear mixed models were used to estimate the overall, interindividual, and intraindividual level independent effects of participation in physical activity on quality of life. Results There was an overall independent association between physical activity and quality of life. At a given time point, participants achieving at least 150 minutes of physical activity per week had an 18% higher quality of life score than those who reported no physical activity. Significant associations were also present at the interindividual level (differences between participants) and intraindividual level (within participant changes). Conclusion These findings suggest that the positive association between physical activity and quality of life is consistent over time. Encouraging colorectal cancer survivors to be physically active may be a helpful strategy for enhancing quality of life.
A cancer diagnosis and subsequent treatment can adversely affect survivors’ quality of life. Common psychological problems encountered by cancer survivors include depression and anxiety, lowered self-esteem, and impaired body image.1 Physical complaints include fatigue, reduced cardiovascular and pulmonary function, muscle weakness and atrophy, pain, difficulty sleeping, and nausea.2 Given the increasing number of people surviving cancer, there is a concomitant interest in how to ameliorate these negative sequelae and hence enhance quality of life for survivors.3,4 Systematic reviews of randomized controlled trials have concluded that physical activity has positive effects on quality-of-life outcomes for cancer survivors.5-7 However, these reviews acknowledge that the findings of many of the trials are not conclusive because of methodologic shortcomings. Physical activity intervention trials have used relatively small clinic-based or other convenience samples, and there has been a preponderance of studies of breast and prostate cancer survivors, limiting the generalization of findings to other cancers. In addition, the interventions have been administered during or shortly after cancer treatment, and few studies have observed participants to evaluate long-term effects. Observational studies allow recruitment of large, population-based samples to provide representative data on the full range of variation in the attributes of interest. A number of observational studies8-12 have found positive associations between physical activity and quality of life. However, most of the studies to date have been cross-sectional; longitudinal data are needed to evaluate whether physical activity has a sustained effect on improvements in quality of life. In the only known prospective study of the impact of physical activity on quality of life involving colorectal cancer survivors, Courneya et al13 assessed 53 participants at approximately 2 months after surgery and again 4 years later. They found that changes in mild-intensity exercise over this period were associated with overall quality of life. Prospective studies of physical activity and quality of life in other cancer populations have also identified positive associations;14-16 however, generalizing these results to colorectal cancer survivors may not be appropriate, as disease characteristics, treatments administered, and demographic characteristics of patients can vary widely between cancer types.7 The aim of the present study is to examine the relationships between physical activity and quality of life in a large sample of colorectal cancer survivors at 6, 12, and 24 months after diagnosis. It is hypothesized that physical activity will be independently and positively associated with quality of life at both inter- and intraindividual levels.
Patient Accrual Data were collected as part of the Colorectal Cancer and Quality of Life Study, the methods of which are described in detail elsewhere.17 In brief, all persons with a histologically confirmed diagnosis of a first, primary colorectal cancer, notified to the Queensland Cancer Registry between January 1, 2003, and December 31, 2004, were eligible for the study. A flow diagram describing recruitment to and participation in the study is shown in Figure 1. The University of Queensland's Behavioral and Social Science Ethical Review Committee approved the study's procedures.
Measures All patients who provided written, informed consent were telephoned by a trained interviewer at approximately 6, 12, and 24 months after diagnosis. Current demographic information, medical treatments, and adverse effects were self-reported at interview. Age, sex, and site and stage of disease were collected from pathology reports held within the Queensland Cancer Registry. Physical activity was assessed using the Active Australia Survey, an instrument used to monitor physical activity participation in the Australian adult population.18,19 Participants reported the amount of time they spent each week walking for transport or recreation, in other moderate-intensity physical activity (eg, gentle swimming, social tennis), and in vigorous-intensity physical activity (eg, jogging, competitive tennis). Total weekly physical activity was calculated by adding together the time spent in each activity category (vigorous activity was double-weighted to account for additional energy expenditure). Current Australian public health guidelines advocate achieving the equivalent of 150 minutes of moderate-intensity activity per week.20 On the basis of these guidelines, participants were categorized as being inactive (0 minutes per week), insufficiently active (1 to 149 minutes per week), or sufficiently active (150 minutes or more per week). The Active Australia Survey demonstrates a moderate level of test-retest reliability (intraclass correlation coefficient, 0.64).21 The Functional Assessment of Cancer Therapy–Colorectal (FACT-C; Version 4) is a 36-item quality-of-life questionnaire with five subscales: physical well-being, social/family well-being, emotional well-being, functional well-being, and colorectal cancer–specific additional concerns. Participants rate how they have felt over the past 7 days, on a scale of 0 ("not at all") to 4 ("very much"). Individual scores are compiled according to a standardized algorithm so that each subscale is scored and then summed to provide an overall quality-of-life score. The overall quality-of-life score can range from 0 to 136 (two items relevant only to stoma patients are not included in the score), with higher scores indicating better quality of life. Each subscale has a maximum score of 28, except for the emotional well-being subscale, which has a maximum of 24. The FACT-C is a valid and reliable measure, sensitive to changes in functional status.22 Changes of between five and eight points are considered the smallest changes of clinical significance for the FACT-C.23
Statistical Analyses Generalized linear mixed models24 with random intercepts were used to estimate the overall independent effects of participation in physical activity on quality of life and to estimate the independent interindividual (differences between participants) and intraindividual (within-participant changes) effects of physical activity on quality of life. Quality of life was modeled as a function of factors specified by a priori hypotheses: sociodemographic, disease-specific variables, treatment adverse effects, body mass index (BMI), time, and physical activity. Given that there were multiple assessments per participant, the models were allowed to have two sources of random variation (or residuals): within-individual and interindividual. Such modeling accounted for the dependency of observations (multiple data from the same individuals). To examine the overall effect of physical activity on quality of life, the measured physical activity variable was entered into the model. To examine the independent inter- and intraindividual effect of physical activity on quality of life, two types of physical activity variables, one representing the interindividual effect, the other representing the intraindividual effect, were simultaneously entered in the models. The interindividual effect was represented by a participant's average amount of physical activity reported during the study across the three measurements. The intraindividual effect was represented by the difference between a participant's physical activity level at a certain point in time and his/her average physical activity level during the study. This variable corresponds to intraindividual changes in physical activity. Models were repeated with variations of the physical activity variable as a categoric variable (sufficiently active and insufficiently active compared with inactive), as a continuous variable (minutes of total activity per week), and as components of total activity (minutes of walking, other moderate-intensity activity, and vigorous-intensity activity per week). Interaction terms were added to each of the models to see whether there were any differences in effect by sex, stage of disease, or BMI. Also, to examine the temporal stability of the associations between physical activity and quality of life across three assessment points, time by physical activity interaction terms were added to the models. The quality-of-life data were negatively skewed, so to adjust for departures from normality, the gamma variance function and log-link functions were used.25 The FACT-C data were reverse-scored so to create a positively skewed distribution and thus provide an acceptable fit to the gamma function. To interpret the regression coefficients obtained under a log-link function, the antilogarithms of the estimated regression coefficients were computed. These represent the expected proportional (percentage) change in outcome after a 1-unit increase in the predictor. P values less than .05 (two-sided) were considered significant.
The characteristics of the sample at each time point, and of nonparticipants, are listed in Table 1. The majority of participants in this study (54%) had surgery as their primary course of treatment, 43% had surgery plus adjuvant therapy (chemotherapy and/or radiation therapy), and 3% had adjuvant therapy only or no treatment.
Comparison of study participants with nonparticipants found no differences in the sex distribution between the groups at any time point. However, the study sample did under-represent older (age 70 to 80 years) colorectal cancer survivors, those with rectal cancer, and those with more advanced disease (  2 test, P < .05 for each). Based on total weekly physical activity, 32% of participants at 6 months after diagnosis were categorized as sufficiently active; in other words, they had accumulated at least 150 minutes of moderate-intensity activity per week. Thirty-seven percent of participants were categorized as sufficiently active at 12 months after diagnosis, and 39% were sufficiently active at 24 months after diagnosis. Table 2 presents mean FACT-C scores for inactive, insufficiently active, and sufficiently active participants, as well as the difference in mean scores between participants in the sufficiently active category and inactive categories.
Model 1: Overall Independent Associations Between Physical Activity and Quality of Life The first generalized linear mixed model examined the overall associations between participation in physical activity and quality of life. When controlling for sociodemographic and disease-specific variables, treatment adverse effects, and time of assessment, categoric physical activity at time t was significantly associated with quality of life at time t. At a given assessment, participants who were sufficiently active (compared with those who were inactive) had an 18% (95% CI, 12% to 23%) higher FACT-C score, whereas participants who were insufficiently active had an 8% (95% CI, 4% to 13%) higher FACT-C than those who were inactive (Table 3). Given the mean quality-of-life scores at each time point, the differences between sufficiently active and inactive participants would have ranged from 20 to 21 points, far exceeding the minimal clinically significant range of five to eight points.
When this model was repeated using the continuous measure of physical activity (total minutes per week), the outcome was also statistically significant. An increase in 10 minutes of physical activity per week was associated with an increase of 0.4% (95% CI, 0.3% to 0.5%) in FACT-C score. In the final variation of this model, physical activity was broken into its components (walking, moderate-intensity activity, and vigorous-intensity activity). Each component had a significant, positive effect on quality of life. It was estimated that increases of 10 minutes per week on each of the components would, on average, yield an increase of approximately 0.3% to 0.5% in FACT-C score. Interaction terms between the various physical activity measures and sex, stage of disease, BMI, and time of assessment were included in the overall independent effects models. There were no significant interactions between physical activity and sex or between physical activity and BMI. Also, no significant moderating effects of time on the associations between physical activity and quality of life were found, indicating that these associations are likely to be stable across time. However, there were significant interactions between continuous physical activity (total minutes per week) and stage of disease (P = .03) and between walking (minutes per week) and stage of disease (P = .04). Total weekly physical activity had a greater effect on quality of life for participants with advanced (stage C or D) disease than for participants with localized (stage A or B) disease. Likewise, walking had a greater effect on quality of life among participants with stage C or D colorectal cancer than for those with stage A or B disease.
Model 2: Independent Inter- and Intraindividual Effects of Physical Activity on Quality of Life
When this model was repeated using the continuous physical activity variable, participants reporting an average of 10 minutes of extra physical activity per week had approximately 0.3% (95% CI, 0.3% to 0.5%) higher FACT-C scores than others (interindividual effect). Participants who increased their total weekly activity by 10 minutes per week reported an increase in quality of life of approximately 0.4% (95% CI, 0.3% to 0.5%). In the final variation of this model, participants who walked more than other participants had higher FACT-C scores (0.4% for each 10 minutes extra; 95% CI, 0.1% to 0.6%), as did those who reported more moderate-intensity activity (0.2% for each 10 minutes extra; 95% CI, 0 to 0.5%). There was no significant main interindividual effect for vigorous-intensity activity. Also, there were no significant interaction effects of physical activity with BMI, sex, and stage of disease on quality of life at the interindividual level. Participants who increased their level of moderate-intensity activity during the study reported concomitant increases in quality of life (0.3% for each 10 minute increase). The effects of changes in walking on quality of life depended on stage of disease (interaction effect P = .04). People diagnosed with advanced (stage C or D) colorectal cancer significantly benefited from changes in walking (0.7% increase in quality of life for each 10-minute increase in walking; 95% CI, 0.3% to 1.1%), whereas people with localized disease did not (0.1% increase in quality of life for each 10-minute increase in walking; 95% CI, –0.3% to 0.5%). Also, the effects of changes in vigorous-intensity activity were moderated by sex (P = .05); increased vigorous physical activity was associated with increased quality of life in women only (1.2% increase for each 10-minute increase; 95% CI, 0.02% to 2.4%). We reran the models presented in Tables 3 and 4 excluding Duke's D participants and found that the association of physical activity with quality of life did not significantly change (they increased 0% to 5%).
This report presents more detailed information about how physical activity is associated with quality of life over time in colorectal cancer survivors than has been previously described. Our findings demonstrate that physical activity is consistently associated with quality of life during the 2 years after diagnosis of colorectal cancer. A significant association was present at the interindividual (between participants) and intraindividual (within participant) level. All measured components of physical activity (walking, moderate-intensity, and vigorous-intensity activity) were important, particularly at the intraindividual levels, although some caution is needed in interpreting the effects of vigorous-intensity physical activity because of the small proportion of patients engaging in it. Although there was a change in BMI between 6 and 12 months after diagnosis, we found no significant interactions between physical activity and BMI in our analyses. This is somewhat surprising given the known associations between physical activity, BMI, and quality of life.26,27 We suggest that the change in BMI between 6 and 12 months from diagnosis may not be due to lifestyle, but instead may reflect a rebound effect after loss of weight before diagnosis and during treatment. Weight loss is a commonly reported symptom of colorectal cancer and an adverse effect of chemotherapy. Hence the BMI values at 6 months after diagnosis may be lower than usual for the study participants, as many will have lost weight from the cancer itself or from associated treatments. By 12 months after diagnosis, most participants are likely to have returned to a more usual (heavier) body mass. Our findings suggest that the positive association between physical activity and quality of life is clinically significant and consistent over time and may be partly causal in nature. However, the results could reflect participants with compromised quality of life being less able or inclined to engage in physical activity in comparison with participants with higher levels of quality of life. Randomized controlled trials are needed to firmly establish causation in the relationship between physical activity and quality of life. We can, however, conclude from this study that participation in physical activity is associated with significantly enhanced quality of life over time (in this case, up to 24 months after diagnosis) for colorectal cancer survivors. These results support the view that promoting participation in physical activity, and particularly promoting regular walking, is a means of enhancing the quality of life of colorectal cancer survivors. The Colorectal Cancer and Quality of Life Study is a comprehensive, population-based study that purposefully included survivors with advanced disease in an attempt to make the sample as representative as possible. However, survivors with advanced disease were less likely to participate in the study. Our sample also under-represented older participants and individuals with rectal cancer. Because of the departures from representativeness in our sample, we expect that the prevalence estimates of physical activity, and quality of life, may be higher than within the true population of colorectal cancer survivors. Another strength of this study was the use of well-tested and validated measures of physical activity and quality of life: the Active Australia Survey18 and the FACT-C.28 Our findings will nonetheless be limited by recall error, social desirability, and other biases inherent in self-report.29,30 Physical activity has long been recognized as beneficial to the health and well-being of people with chronic diseases, such as cardiovascular disease and diabetes. There is now a strong interest in the potential role of physical activity in the rehabilitation of cancer survivors.7,31 Our study supports the case that individuals should be encouraged to participate in physical activity after a diagnosis of colorectal cancer.
The author(s) indicated no potential conflicts of interest.
Conception and design: Brigid M. Lynch, Neville Owen, Joanne F. Aitken Administrative support: Brigid M. Lynch, Anna L. Hawkes Collection and assembly of data: Brigid M. Lynch Data analysis and interpretation: Brigid M. Lynch, Ester Cerin Manuscript writing: Brigid M. Lynch, Ester Cerin, Neville Owen, Anna L. Hawkes, Joanne F. Aitken Final approval of manuscript: Brigid M. Lynch, Ester Cerin, Neville Owen, Anna L. Hawkes, Joanne F. Aitken
Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Int J Obes Relat Metab Disord 25:914-919, 2001[Medline] 30. Sallis JF, Saelens BE: Assessment of physical activity by self-report: Status, limitations, and future directions. Res Q Exerc Sport 71:S1-S14, 2000 (suppl)[Medline] 31. Oldervoll LM, Kaasa S, Hjermstad MJ, et al: Physical exercise results in the improved subjective well-being of a few or is effective rehabilitation for all cancer patients? Eur J Cancer 40:951-962, 2004[CrossRef][Medline] Submitted December 12, 2007; accepted May 20, 2008.
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Copyright © 2008 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
